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Patterns and Drivers of Deep Chlorophyll Maxima Structure in 100 Lakes: the Relative Importance of Light and Thermal Stratification

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Patterns and Drivers of Deep Chlorophyll Maxima Structure in 100 Lakes: the Relative Importance of Light and Thermal Stratification LIMNOLOGY and Limnol. Oceanogr. 63, 2018, 628–646 VC 2017 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. OCEANOGRAPHY on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10656 Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: The relative importance of light and thermal stratification Taylor H. Leach ,1,a* Beatrix E. Beisner ,2 Cayelan C. Carey ,3 Patricia Pernica,2 Kevin C. Rose ,4 Yannick Huot ,5 Jennifer A. Brentrup ,1 Isabelle Domaizon ,6 Hans-Peter Grossart ,7,8 Bastiaan W. Ibelings ,9 Stephan Jacquet,6 Patrick T. Kelly ,1 James A. Rusak ,10,11 Jason D. Stockwell,12 Dietmar Straile ,13 Piet Verburg 14 1Department of Biology, Miami University, Oxford, Ohio 2Department of Biological Sciences, University of Quebec at Montreal and Groupe de Recherche Interuniversitaire en Limnologie (GRIL), Montreal, Quebec, Canada 3Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 4Department of Biological Sciences, Rensselaer Polytechnic Institute, Troy, New York 5Departement de geomatique appliquee, University of Sherbrooke, Sherbrooke, Quebec, Canada 6INRA, UMR CARRTEL, Thonon les Bains cx, France 7Department Experimental Limnology, Leibniz Institute for Freshwater Ecology and Inland Fisheries, Stechlin, Germany 8Institute for Biochemistry and Biology, Potsdam University, Potsdam, Germany 9Institute F.-A.- Forel and Institute for Environmental Sciences, University of Geneva, Geneva, Switzerland 10Dorset Environmental Science Centre, Ontario Ministry of the Environment and Climate Change, Dorset, Ontario, Canada 11Department of Biology, Queen’s University, Kingston, Ontario, Canada 12Rubenstein Ecosystem Science Laboratory, University of Vermont, Burlington, Vermont 13Limnological Institute, University of Konstanz, Konstanz, Germany 14National Institute of Water and Atmospheric Research, Hamilton, New Zealand Abstract The vertical distribution of chlorophyll in stratified lakes and reservoirs frequently exhibits a maximum peak deep in the water column, referred to as the deep chlorophyll maximum (DCM). DCMs are ecologically important hot spots of primary production and nutrient cycling, and their location can determine vertical habitat gradients for primary consumers. Consequently, the drivers of DCM structure regulate many charac- teristics of aquatic food webs and biogeochemistry. Previous studies have identified light and thermal stratifi- cation as important drivers of summer DCM depth, but their relative importance across a broad range of lakes is not well resolved. We analyzed profiles of chlorophyll fluorescence, temperature, and light during summer stratification from 100 lakes in the Global Lake Ecological Observatory Network (GLEON) and quan- tified two characteristics of DCM structure: depth and thickness. While DCMs do form in oligotrophic lakes, we found that they can also form in eutrophic to dystrophic lakes. Using a random forest algorithm, we assessed the relative importance of variables associated with light attenuation vs. thermal stratification for predicting DCM structure in lakes that spanned broad gradients of morphometry and transparency. Our anal- yses revealed that light attenuation was a more important predictor of DCM depth than thermal stratification and that DCMs deepen with increasing lake clarity. DCM thickness was best predicted by lake size with larger lakes having thicker DCMs. Additionally, our analysis demonstrates that the relative importance of light and thermal stratification on DCM structure is not uniform across a diversity of lake types. *Correspondence: [email protected] aPresent address: Department of Biological Sciences, Rensselaer Polytechnic The vertical distribution of phytoplankton chlorophyll in Institute, Troy, New York lakes and oceans frequently exhibits a peak deep in the Additional Supporting Information may be found in the online version water column, referred to as the deep chlorophyll maximum of this article. or DCM (e.g., Fee 1976; Williamson et al. 1996a; Mignot This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in et al. 2011; Silsbe and Malkin 2016). DCMs can account for any medium, provided the original work is properly cited. as much as 60% of areal primary production in oligotrophic 628 Leach et al. Patterns and drivers of DCM structure across lakes lakes and oceans (Moll et al. 1984; Weston et al. 2005; reported as 1–3% of incident surface photosynthetically Giling et al. 2017) and influence nutrient cycling (Jamart active radiation (PAR; Fee 1976; Banse 1987, 2004; Perez et al. 1977; Letelier et al. 2004). DCMs create a vertical et al. 2002; Morel et al. 2007), or as daily integrated PAR val- resource gradient for primary consumers and thus influence ues of 0.1–1.2 mol quanta m22 d21 (Letelier et al. 2004; zooplankton vertical distributions and diel vertical migration Mignot et al. 2014). (Williamson et al. 1996a; Winder et al. 2003), as well as Other characteristics of DCM structure, aside from DCM predator aggregations (Tiselius et al. 1993). Additionally, depth, have received far less attention. Though analytical DCMs are often associated with elevated densities of mixo- definitions have varied, DCM thickness is generally defined trophic (Bird and Kalff 1989) and heterotrophic (Dolan and as the depth range over which a Chl peak occurs (Platt et al. Marrase 1995) protozoans, and bacterial biomass that can be 1988; Beckmann and Hense 2007; Hanson et al. 2007; Jobin 10X greater than elsewhere in the water column (Auer and and Beisner 2014). DCM thickness can be quantified as the Powell 2004). Consequently, the presence and characteristics depth range where Chl values are within a certain percent- of DCMs, such as their depth or size, can have important age of the maximum Chl concentration (e.g., Jobin and Beis- implications for predator–prey interactions, biogeochemistry, ner 2014), or where a certain percentage of the integrated and energy flow in aquatic ecosystems. Chl occurs (e.g., Platt et al. 1988). Although, when specifi- Many characteristics contribute to regulating the depth of cally considering deep biomass layers, the depth range of net DCM formation in lakes (Durham and Stocker 2012; Cullen primary production can also be used (Beckmann and Hense 2015). Light availability, the vertical distribution of 2007). nutrients, and the location of thermal gradients in the water The few studies that have examined factors controlling column are frequently identified as the main abiotic drivers DCM thickness have concluded that DCMs are thinner and of the depth of DCM formation (e.g., Fee 1976; Abbott et al. more sharply peaked with stronger stratification at the depth 1984). DCMs form because phytoplankton must balance at which they develop (i.e., where the relative availability of opposing gradients of light from above with the availability light vs. nutrients is optimized; Varela et al. 1994; Mellard of nutrients, which often increase with depth under strati- et al. 2011). In areas of strong stratification, non-motile cells fied conditions (Abbott et al. 1984; Carney et al. 1988; Clegg are hypothesized to aggregate in thin layers by sinking or ris- et al. 2007; Descy et al. 2010). Other biological factors can ing to the depths of neutral buoyancy (Alldredge et al. 2002; contribute to DCM formation, including high in situ growth Durham and Stocker 2012). Once these cells reach neutral at depth (Coon et al. 1987; Lande et al. 1989), or behavioral buoyancy, vertical dispersion is inhibited by the strong den- aggregations to nutrient-replete depths via physiological- sity gradient and in situ growth (Lande et al. 1989) and pho- influenced swimming in motile species (Durham and Stocker toacclimation (Fennel and Boss 2003) may further contribute 2012), or buoyancy-controlled movements in non-motile to high Chl concentrations over a small vertical depth range. species (e.g., Oliver 1994; Villareal et al. 1996). Horizontal Theoretical models predict that the exponential decay of movement of water masses such as intrusions or those that light in the water column, combined with a gradient of cause shear may also contribute to DCM formation by later- nutrient concentrations below the thermocline, means that ally transporting deep, nutrient- or phytoplankton-replete optimal conditions for high phytoplankton growth can exist waters (Durham and Stocker 2012). Under oligotrophic con- over an increasingly broad depth range with increasing lake ditions, DCMs may also form independently of phytoplank- transparency, which may also influence DCM thickness ton biomass peaks due to increased chlorophyll (Chl) per (Beckmann and Hense 2007). However, because our under- unit biomass because in these highly transparent lakes suffi- standing of mechanistic controls of DCM thickness primarily cient light may penetrate to depths with relatively higher stems from theoretical modeling (e.g., Varela et al. 1994; nutrient conditions, a process known as photoacclimation or Beckmann and Hense 2007; Mellard et al. 2011), not empiri- photoadaptation (Fennel and Boss 2003). These mechanisms cal studies (but see Mignot et al. 2011), the way in which are not mutually exclusive and may act in concert to con- these mechanisms interact across broad gradients of lake tribute to the formation of a DCM (Mignot et al. 2014). morphometry and transparency remains an open question. Thermal stratification determines DCM depth because it
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